Araştırma Makalesi
BibTex RIS Kaynak Göster

Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs

Yıl 2024, Cilt: 28 Sayı: 3, 505 - 516, 30.06.2024
https://doi.org/10.16984/saufenbilder.1376028

Öz

Staphylococcus aureus (S. aureus) is bacterium that threatens public health because it causes infections and food intoxication. For this reason, within the scope of this study, it was aimed to determine the presence of S. aureus, antibiotic resistance profiles, and biofilm formation in ground beef and meatball samples consumed in Amasya. In the study, 60 meat samples purchased from Amasya were used as material. First, conventional culture technique and PCR testing were used for the isolation of S. aureus. Secondly, antibiotic resistance profiles of the S. aureus were analyzed by disc diffusion. Finally, biofilm production of the S. aureus was analyzed phenotypically by the microtiter plate method and genotypically by PCR. Through the study, we identified 58 S. aureus isolates that were confirmed phenotypically and genotypically. Disc diffusion results showed that all S. aureus were sensitive to imipenem and piperacillin-tazobactam, but resistant to methicillin 43.10% (25/58), erythromycin 41.37 % (24/58), penicillin 58.62% (34/58), gentamicin 10.34% (6/58), chloramphenicol 17.24% (10/58), tobramycin 6.89% (4/58), and levofloxacin 1.72% (1/58). Biofilm production was determined as 58.62% (34/58) in the microtiter plate. In the PCR analysis, the icaA or icaD gene of a total of 4 (6.89%) different isolates was evaluated as positive. As a result, the presence of antibiotic-resistant S. aureus in ground beef and meatballs and the production of biofilm by the bacteria pose a potential risk. Therefore, it is important for human health to take the necessary precautions to reduce the risk of S. aureus contamination during the processing, and transportation.

Kaynakça

  • [1] S. Parvin, Y. Ali, S. Talukder, A. Nahar, E. H. Chowdhury, T. Rahman, T. Islam, “Prevalence and multidrug resistance pattern of methicillin resistant S. aureus isolated from frozen chicken meat in Bangladesh,” Microorganisms, vol. 9, no. 3, pp. 636, 2021.
  • [2] S. Karimi, H. Momtaz, “Molecular typing, phenotypic and genotypic assessment of antibiotic resistance and virulence factors amongst the Staphylococcus aureus bacteria isolated from raw chicken meat,” Molecular Genetics, Microbiology and Virology, vol. 37, no. 4, pp. 226-241, 2022.
  • [3] D. Bae, D. M. Macoy, W. Ahmad, S. Peseth, B. Kim, J. W. Chon, G. R. Ryu, G. H. Ban, S. A. Kim, H. J. Kang, J. S. Moon, M. G. Kim, “Distribution and characterization of antimicrobial resistant pathogens in a pig farm, slaughterhouse, meat processing plant, and in retail stores,” Microorganisms, vol. 10, no. 11, pp. 2252, 2022.
  • [4] World Health Organization (2021), “Global Antimicrobial Resistance and Use Surveillance System (GLASS)”, Available at: https://www.who.int/publications/i/ item/9789240027336.
  • [5] Q. Tao, Q. Wu, Z. Zhang, J. Liu, C. Tian, Z. Huang, P. K. Malakar, Y. Pan, Y. Zhao, “Meta-analysis for the global prevalence of foodborne pathogens exhibiting antibiotic resistance and biofilm formation,” Frontiers in Microbiology, vol. 13, pp. 906490, 2022.
  • [6] J. Kim, J. Ahn, “Emergence and spread of antibiotic-resistant foodborne pathogens from farm to table,” Food Science and Biotechnology, vol. 31, no. 12, pp.1481-1499, 2022.
  • [7] V. K. Ahmed, I. M. Helal, M. M. Zaky, M. Abdulla, “Antimicrobial activity of Actinomycetes extracts against multidrug-resistant Staphylococcus aureus and Salmonella spp. isolated from meat,” Alfarama Journal of Basic & Applied Sciences, vol. 3, no. 2, pp. 283-299, 2022.
  • [8] T. Asfaw, D. Genetu, D. Shenkute, T. Shenkutie, Y. E. Amare, B. Yitayew, “High levels of multidrug-resistant and beta-lactamase-producing bacteria in meat and meat contact surfaces, Debre Berhan Town, Ethiopia,” Infection and Drug Resistance, vol. 16, no. 1, pp. 1965-1977, 2023.
  • [9] M. G. Basanisi, G. Nobili, G. La Bellaa, R. Russo, G, Spano, G. Normanno, G. La Salandraa, “Molecular characterization of Staphylococcus aureus isolated from sheep and goat cheeses in southern Italy,” Small Ruminant Research, vol. 135, pp. 17-19, 2016.
  • [10] A. Fetsch, S. Joler, “Staphylococcus aureus as a foodborne pathogen,” Current Clinical Microbiology Reports, vol. 5, pp. 88–96, 2018.
  • [11] M. Yousefi, M. Farshidi, M. A. Sani, L. Payahoo, “Investigation of the microbial quality and the occurrence of Shiga-like-toxin-producing Escherichia coli and methicillin resistant Staphylococcus aureus in traditional cheeses produced in northwest of Iran,” Nutrition & Food Science, vol. 3, pp. 407-417, 2018.
  • [12] S. Gürbüz, Ç. Güngör, “Determination of some foodborne pathogens and residual nitrate and nitrite in traditional fermented sausages in Turkey,” International Food Research Journal, vol. 27, no. 1, pp. 39-46. 2020.
  • [13] P. Visciano, F. Pomilio, R. Tofalo, L. Sacchini M. A Saletti, E. Tieri, M. Schirone, G. Suzzi, “Detection of methicillin resistant Staphylococcus aureus in dairy cow farms,” Food Control, vol. 46, pp. 532-538, 2014.
  • [14] J. M. Kwiecinski, A. R. Horswill, “Staphylococcus aureus bloodstream infections: pathogenesis and regulatory mechanisms,” Current Opinion in Microbiology, vol. 53, pp. 51-60, 2020.
  • [15] P. Şanlıbaba, “Prevalence, antibiotic resistance, and enterotoxin production of Staphylococcus aureus isolated from retail raw beef, sheep, and lamb meat in Turkey,” Internatol Journal Food Microbiology, vol. 361, pp. 109461, 2022.
  • [16] W. Sankomkai, W. Boonyanugomol, K. Kraisriwattana, J. Nutchanon, K. Boonsam, S. Kaewbutra, W. Wongboot, “Characterisation of classical enterotoxins, virulence activity, and antibiotic susceptibility of isolated from Thai fermented pork sausages, clinical samples, and healthy carriers in northeastern Thailand,” Journal of Veterinary Research, vol. 64, no. 2, pp. 289-297, 2020.
  • [17] G. K. Sivaraman, S. S. Grupta, S. Visnuvinayagam, T. Muthulakshmi, R. Elangovan, V. Perumal, G. Balasubramanium, T. Lodha, A. Yadav, “Prevalence of S. aureus and/or MRSA from seafood products from Indian seafood products,” BMC Microbiology, vol. 22, no. 1, pp. 233, 2022.
  • [18] N. Guo, B. Xue, Y. Shen, T. Zhang, “Target-based screening for natural products against Staphylococcus aureus biofilms,” Critical reviews in Food Science and Nutrition, vol. 63, no. 14, pp. 2216-2230,2023.
  • [19] M. T. Kashef, N. M. Saleh, N. H. Assar, M. A. Ramadan, “The antimicrobial activity of ciprofloxacin-loaded niosomes against ciprofloxacin-resistant and biofilm-forming Staphylococcus aureus,” Infection and Drug Resistance, vol. 13, pp. 1619-1629, 2020.
  • [20] S. Derakhshan, M. Navidinia, F. Haghi, “Antibiotic susceptibility of human associated Staphylococcus aureus and its relation to agr typing, virulence genes, and biofilm formation,” BMC Infectious Diseases, vol. 21, pp. 627, 2021.
  • [21] C. Wang, Y. Xiong, C. Bao, Y. Wei, Z. Wen, X. Cao, Z. Yu, X. Deng, G. Li, Q. Deng, “Antibacterial and anti-biofilm activity of radezolid against Staphylococcus aureus clinical isolates from China,” Frontiers in Microbiology, vol. 14, pp. 1131178, 2023.
  • [22] J. Gajewska, W. Chajecka-Wierzchowska, “Biofilm formation ability and presence of adhesion genes among coagulase-negative and coagulase-positive Staphylococci isolates from raw cow’s milk,” Pathogens, vol. 9, no. 8, pp. 654, 2020.
  • [23] J. Gajewska, W. C. Wierzchowska, A. Zadernowska, “Occurrence and characteristics of Staphylococcus aureus strains along the production chain of raw milk cheeses in Poland,” Molecules, vol. 27, no. 19, pp. 6569, 2022.
  • [24] D. Ashraf, R. A. Ombarak, A. Samir, A. B. Abdel-Salam, “Characterization of multidrug-resistant potential pathogens isolated from milk and some dairy products in Egypt,” Journal of Advanced Veterınary and Animal Research, vol. 10, no. 2, pp. 275-283, 2023.
  • [25] T. Cebeci, N. Gündoğan, “Enterotoxin production and antibiotic resistance profile of Staphylococcus aureus isolated from meat samples,” Hitit Medical Journal, vol. 3, no. 2, 13-19, 2021.
  • [26] K. Abbasi, E. Tajbakhsh, H. Momtaz, “Antimicrobial resistance, virulence genes, and biofilm formation in Staphylococcus aureus strains isolated from meat and meat products,” Journal of food safety, vol. 41, no. 2, pp. 1-10, 2021.
  • [27] S. Yoon, Y. K. Park, T. S. Jung, S. B. Park, “Molecular typing, antibiotic resistance and enterotoxin gene profiles of Staphylococcus aureus isolated from humans in South Korea,” Microorganisms, vol. 10, no. 3, pp. 642, 2022.
  • [28] K. Zhang, J. Sarling, B. L. Chow, S. Elsayed, Z. Hussain, D. L. Church, D. B. Gregson, T. Louie, J. M. Conly, “New quadriplex PCR assay for detection of methicillin resistance and simultaneous discrimination of S. aureus from coagulase-negative Staphylococci,” Journal Clinical Microbiology, vol. 42, no. 11, pp. 4947-4955, 2004.
  • [29] J. A. McClure, J. M. Conly, V. Lau, S. Elsayed, T. Louie, W. Hutchins, K. Zhang, “Novel multiplex PCR assay for detection of the Staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from resistant Staphylococci,” Journal Clinical Microbiology, vol. 44, no. 3, pp. 1141-1144, 2006.
  • [30] P. Vasudevan, M. K. M. Nair, T. Annamalai, K. S. Venkitanarayanan, “Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation,” Veterinary Microbiology, vol. 92, no. 1-2, pp.179-185, 2003.
  • [31] Clinical laboratory standart institute, (CLSI), “Performance Standards for antimicrobial susceptibility testing. Twentieth edition,” Informational Supplement M100-S22, Wayne, PA, 2012.
  • [32] T. Saba, M. Sajid, A. A. Khan, R. Zahra, “Role of intracellular adhesion icaAD and agr genes in biofilm formation in clinical S. aureus isolates and assessment of two phenotypic methods,” Pakistan Journal of Medical Science, vol. 34, no. 3, pp. 633-637, 2018.
  • [33] K. Kolodziejczak, A. Onopiuk, A. Szpicer, A. Poltorak, “Meat analogues in the perspective of recent scientific research: a review,” Foods, vol. 11, no. 1, pp. 105, 2022.
  • [34] L. Grispoldi, P. A. Popescu, M. Karama, V. Gullo, G. Poerio, E. Borgogni, P. Torlai, G. Chianese, A. G. Fermani, P. Sechi, B. Cenci-Goga, “Study on the growth and enterotoxin production by Staphylococcus aureus in canned meat before retorting,” Toxins, vol. 11, no. 5, pp. 291, 2019.
  • [35] T. Thwala, E. Madoroba, A. Basson, P. Butaye, “Prevalence and characteristics of Staphylococcus aureus associated with meat and meat products in African countries: a review,” Antibiotics, vol. 10, no. 9, pp. 1108, 2021.
  • [36] E. O. Igbinosa, A. Beshiru, I. H. Igbinosa, A. G. Ogofure, T. C. Ekundayo, A. I. Okoh, “Prevalence, multiple antibiotic resistance and virulence profile of methicillin resistant Staphylococcus aureus (MRSA) in retail poultry meat from Edo, Nigeria,” Frontiers in Cellular and Infection Microbiology, vol. 13, pp. 1122059, 2023.
  • [37] D. Komodromos, C. Kotzamanidis, V. Giantzi, S. Pappa, A. Papa, A. Zdragas, A. Angelidis, D. Sergelidis, “Prevalence, infectious characteristics and genetic diversity of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) in two raw-meat processing establishments in Northern Greece,” Pathogens, vol. 11, no. 11, pp. 1370, 2022.
  • [38] M. Rajaei, M. H. Moosavy, S. N. Gharajalar, S. A. Khatibi, “Antibiotic resistance in the pathogenic foodborne bacteria isolated from raw kebab and hamburger: phenotypic and genotypic study,” BMC Microbiology, vol. 21, pp. 272, 2021.
  • [39] E. Keyvan, H. Özdemir, “Sığır karkaslarında Staphylococcus aureus’un varlığı, enterotoksijenik özellikleri ve antimikrobiyal dirençliliği,” Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 63, pp. 17-23, 2016.
  • [40] N. Gündoğdu, A. Devren, “Protease and lipase activity of Staphylococcus aureus obtained from meat, chicken and meatball samples,” Gazi University Journal of Science, vol. 23, no. 4, pp. 381-384, 2010.
  • [41] M. H. Chaia, T. A. M. Faiqa, S. M. Z. Ariffinb, Z. Suhailia, M. Z. Sukimana, M. F. Ghazali, “Prevalence of methicillin resistant Staphylococcus aureus in raw goat milks from selected farms in Terengganu, Malaysia,” Tropical Animal Science Journal, vol. 43, no. 1, pp. 64-69, 2020.
  • [42] A. M. Edris, A. A. A. Maarouf, R. A. E. Amin, E. A. I. Bahbah, “Prevalence of Staphylococci in meat products with special reference to methicillin-resistant Staphylococcus aureus (MRSA) at Kaliobia Governorate,” Benha Veterinary Medical Journal, vol. 35, no. 2, pp. 364-374, 2018.
  • [43] G. A. Ballash, A. L. Albers, D. F. Mollenkopf, E. Sechrist, R. J. Adams, T. E. Wittum, “Antimicrobial resistant bacteria recovered from retail ground meat products in the US include a Raoultella ornithinolytica co-harboring blaKPC-2 and blaNDM-5,” Scientific Reports, vol. 11, pp. 14041, 2021.
  • [44] S. Wu, J. Huang, Q. Wu, J. Zhang, F. Zhang, X. Yang, H. Wu, H. Zeng, M. Chen, Y. Ding, J. Wang T. Lei, S. Zhang, L. Xue, “Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity,” Frontiers in Microbiology, vol. 9, pp. 2767, 2018.
  • [45] M. G. Basanisi, G. La Bella, G. Nobili, S. Tola, M. A. Cafiero, G. La Salandra, “Prevalence and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from retail meat in south Italy,” Italian Journal of Food Science, vol. 32, no. 2, pp. 410-419, 2020.
  • [46] Z. T. Baghbaderani, A. Shakerian, E. Rahimi, “Phenotypic and genotypic assessment of antibiotic resistance of Staphylococcus aureus bacteria isolated from retail meat,” Infection and Drug Resistance, vol. 13, pp. 1339-1349, 2020.
  • [47] D. A. Hasanpour, L. Khaji, S. M. Sakhaei, Z. Mashak, D. F. Safarpoor, Y. Safaee, A. Hosseinzadeh, I. Alavi, E. Ghasem, F. M. Rabiei, “One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat,” Tropical Biomedicine, vol. 34, no. 2, pp. 396-404, 2017.
  • [48] P. Fowoyo, S. Ogunbanwo, “Antimicrobial resistance in coagulase-negative Staphylococci from Nigerian traditional fermented foods,” Annals of Clinical Microbiology and Antimicrobial, vol. 16, no. 4, pp. 1-7, 2017.
  • [49] A. Kılıç, E. Doğan, S. Kaya, M. Baysallar, “Yedi yıllık sürede klinik örneklerden izole edilen Staphylococcus aureus suşlarında mecC ve Panton-Valantine lökosidin gen varlığının araştırılması,” Mikrobiyoloji Bülteni, vol. 49, no. 4, pp. 594-599, 2015.
  • [50] R. Parastan, M. Kargara, K. Solhjooc, F. Kafilzadeh, “Staphylococcus aureus biofilms: structures, antibiotic resistance, inhibition, and vaccines,” Gene Reports, vol. 20, pp. 100739, 2020.
  • [51] A. C. Silva-de-Jesus, R. G. Ferrari, P. Panzenhagen, C. A. ConteJunior, “Staphylococcus aureus biofilm: the role in disseminating antimicrobial resistance over the meat chain,” Microbiology, vol. 168, pp. 001245, 2022.
  • [52] L. E. Alcaraz, S. E. Satorres, R. M. Lucero, O. N. P. Centorbi, “Species identification, slime production and oxacillin susceptibility in coagulase-negative staphylococci isolated from nosocomial specimens,” Brazilian Journal of Microbiology, vol. 34, no. 1, pp. 45-51, 2003.
  • [53] A. Ciftci, A. Findik, E. E. Onuk, S. Savasan, “Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis,” Brazilian Journal of Microbiology, vol. 40, no. 2, pp. 254-261, 2009.
  • [54] A. Prenafeta, M. Sitjà, M. A. Holmes, G. K. Paterson, “Communication: Biofilm production characterization of mecA and mecC methicillin-resistant Staphylococcus aureus isolated from bovine milk in Great Britain,” Journal of Dairy Science, vol. 97, pp. 4838–4841, 2014.
  • [55] A. E. M. A. Morshdy, A. E. Tharwat, A. M. A. Merwad, N. A. M. Abdallah, T. Saber, “Prevalence, phenotypic-genotypic resistance and biofilm formation of Staphylococcus aureus in chicken meat with reference to its public health hazard,” Veterinary Medicine and The One Health Concept, vol. 60, pp. 413–424, 2023.
  • [56] M. E. A. Bissong, C. N. Ateba, “Genotypic and phenotypic evaluation of biofilm production and antimicrobial resistance in Staphylococcus aureus isolated from milk, NorthWest province, South Africa,” Antibiotics, vol. 9, pp. 156, 2020.
  • [57] M. G. Avila-Novoa, M. Iñıguez-Moreno, O. A. Solıs-Velazquez, J. P. Gonzalez-Gomez, P. J. Guerrero-Medina, M. Gutierrez-Lomel, “Biofilm Formation by Staphylococcus aureus isolated from Food Contact Surfaces in the Dairy Industry of Jalisco, Mexico,” Journal of Food Quality, vol. 2018, pp. 1746139, 2018.
Yıl 2024, Cilt: 28 Sayı: 3, 505 - 516, 30.06.2024
https://doi.org/10.16984/saufenbilder.1376028

Öz

Kaynakça

  • [1] S. Parvin, Y. Ali, S. Talukder, A. Nahar, E. H. Chowdhury, T. Rahman, T. Islam, “Prevalence and multidrug resistance pattern of methicillin resistant S. aureus isolated from frozen chicken meat in Bangladesh,” Microorganisms, vol. 9, no. 3, pp. 636, 2021.
  • [2] S. Karimi, H. Momtaz, “Molecular typing, phenotypic and genotypic assessment of antibiotic resistance and virulence factors amongst the Staphylococcus aureus bacteria isolated from raw chicken meat,” Molecular Genetics, Microbiology and Virology, vol. 37, no. 4, pp. 226-241, 2022.
  • [3] D. Bae, D. M. Macoy, W. Ahmad, S. Peseth, B. Kim, J. W. Chon, G. R. Ryu, G. H. Ban, S. A. Kim, H. J. Kang, J. S. Moon, M. G. Kim, “Distribution and characterization of antimicrobial resistant pathogens in a pig farm, slaughterhouse, meat processing plant, and in retail stores,” Microorganisms, vol. 10, no. 11, pp. 2252, 2022.
  • [4] World Health Organization (2021), “Global Antimicrobial Resistance and Use Surveillance System (GLASS)”, Available at: https://www.who.int/publications/i/ item/9789240027336.
  • [5] Q. Tao, Q. Wu, Z. Zhang, J. Liu, C. Tian, Z. Huang, P. K. Malakar, Y. Pan, Y. Zhao, “Meta-analysis for the global prevalence of foodborne pathogens exhibiting antibiotic resistance and biofilm formation,” Frontiers in Microbiology, vol. 13, pp. 906490, 2022.
  • [6] J. Kim, J. Ahn, “Emergence and spread of antibiotic-resistant foodborne pathogens from farm to table,” Food Science and Biotechnology, vol. 31, no. 12, pp.1481-1499, 2022.
  • [7] V. K. Ahmed, I. M. Helal, M. M. Zaky, M. Abdulla, “Antimicrobial activity of Actinomycetes extracts against multidrug-resistant Staphylococcus aureus and Salmonella spp. isolated from meat,” Alfarama Journal of Basic & Applied Sciences, vol. 3, no. 2, pp. 283-299, 2022.
  • [8] T. Asfaw, D. Genetu, D. Shenkute, T. Shenkutie, Y. E. Amare, B. Yitayew, “High levels of multidrug-resistant and beta-lactamase-producing bacteria in meat and meat contact surfaces, Debre Berhan Town, Ethiopia,” Infection and Drug Resistance, vol. 16, no. 1, pp. 1965-1977, 2023.
  • [9] M. G. Basanisi, G. Nobili, G. La Bellaa, R. Russo, G, Spano, G. Normanno, G. La Salandraa, “Molecular characterization of Staphylococcus aureus isolated from sheep and goat cheeses in southern Italy,” Small Ruminant Research, vol. 135, pp. 17-19, 2016.
  • [10] A. Fetsch, S. Joler, “Staphylococcus aureus as a foodborne pathogen,” Current Clinical Microbiology Reports, vol. 5, pp. 88–96, 2018.
  • [11] M. Yousefi, M. Farshidi, M. A. Sani, L. Payahoo, “Investigation of the microbial quality and the occurrence of Shiga-like-toxin-producing Escherichia coli and methicillin resistant Staphylococcus aureus in traditional cheeses produced in northwest of Iran,” Nutrition & Food Science, vol. 3, pp. 407-417, 2018.
  • [12] S. Gürbüz, Ç. Güngör, “Determination of some foodborne pathogens and residual nitrate and nitrite in traditional fermented sausages in Turkey,” International Food Research Journal, vol. 27, no. 1, pp. 39-46. 2020.
  • [13] P. Visciano, F. Pomilio, R. Tofalo, L. Sacchini M. A Saletti, E. Tieri, M. Schirone, G. Suzzi, “Detection of methicillin resistant Staphylococcus aureus in dairy cow farms,” Food Control, vol. 46, pp. 532-538, 2014.
  • [14] J. M. Kwiecinski, A. R. Horswill, “Staphylococcus aureus bloodstream infections: pathogenesis and regulatory mechanisms,” Current Opinion in Microbiology, vol. 53, pp. 51-60, 2020.
  • [15] P. Şanlıbaba, “Prevalence, antibiotic resistance, and enterotoxin production of Staphylococcus aureus isolated from retail raw beef, sheep, and lamb meat in Turkey,” Internatol Journal Food Microbiology, vol. 361, pp. 109461, 2022.
  • [16] W. Sankomkai, W. Boonyanugomol, K. Kraisriwattana, J. Nutchanon, K. Boonsam, S. Kaewbutra, W. Wongboot, “Characterisation of classical enterotoxins, virulence activity, and antibiotic susceptibility of isolated from Thai fermented pork sausages, clinical samples, and healthy carriers in northeastern Thailand,” Journal of Veterinary Research, vol. 64, no. 2, pp. 289-297, 2020.
  • [17] G. K. Sivaraman, S. S. Grupta, S. Visnuvinayagam, T. Muthulakshmi, R. Elangovan, V. Perumal, G. Balasubramanium, T. Lodha, A. Yadav, “Prevalence of S. aureus and/or MRSA from seafood products from Indian seafood products,” BMC Microbiology, vol. 22, no. 1, pp. 233, 2022.
  • [18] N. Guo, B. Xue, Y. Shen, T. Zhang, “Target-based screening for natural products against Staphylococcus aureus biofilms,” Critical reviews in Food Science and Nutrition, vol. 63, no. 14, pp. 2216-2230,2023.
  • [19] M. T. Kashef, N. M. Saleh, N. H. Assar, M. A. Ramadan, “The antimicrobial activity of ciprofloxacin-loaded niosomes against ciprofloxacin-resistant and biofilm-forming Staphylococcus aureus,” Infection and Drug Resistance, vol. 13, pp. 1619-1629, 2020.
  • [20] S. Derakhshan, M. Navidinia, F. Haghi, “Antibiotic susceptibility of human associated Staphylococcus aureus and its relation to agr typing, virulence genes, and biofilm formation,” BMC Infectious Diseases, vol. 21, pp. 627, 2021.
  • [21] C. Wang, Y. Xiong, C. Bao, Y. Wei, Z. Wen, X. Cao, Z. Yu, X. Deng, G. Li, Q. Deng, “Antibacterial and anti-biofilm activity of radezolid against Staphylococcus aureus clinical isolates from China,” Frontiers in Microbiology, vol. 14, pp. 1131178, 2023.
  • [22] J. Gajewska, W. Chajecka-Wierzchowska, “Biofilm formation ability and presence of adhesion genes among coagulase-negative and coagulase-positive Staphylococci isolates from raw cow’s milk,” Pathogens, vol. 9, no. 8, pp. 654, 2020.
  • [23] J. Gajewska, W. C. Wierzchowska, A. Zadernowska, “Occurrence and characteristics of Staphylococcus aureus strains along the production chain of raw milk cheeses in Poland,” Molecules, vol. 27, no. 19, pp. 6569, 2022.
  • [24] D. Ashraf, R. A. Ombarak, A. Samir, A. B. Abdel-Salam, “Characterization of multidrug-resistant potential pathogens isolated from milk and some dairy products in Egypt,” Journal of Advanced Veterınary and Animal Research, vol. 10, no. 2, pp. 275-283, 2023.
  • [25] T. Cebeci, N. Gündoğan, “Enterotoxin production and antibiotic resistance profile of Staphylococcus aureus isolated from meat samples,” Hitit Medical Journal, vol. 3, no. 2, 13-19, 2021.
  • [26] K. Abbasi, E. Tajbakhsh, H. Momtaz, “Antimicrobial resistance, virulence genes, and biofilm formation in Staphylococcus aureus strains isolated from meat and meat products,” Journal of food safety, vol. 41, no. 2, pp. 1-10, 2021.
  • [27] S. Yoon, Y. K. Park, T. S. Jung, S. B. Park, “Molecular typing, antibiotic resistance and enterotoxin gene profiles of Staphylococcus aureus isolated from humans in South Korea,” Microorganisms, vol. 10, no. 3, pp. 642, 2022.
  • [28] K. Zhang, J. Sarling, B. L. Chow, S. Elsayed, Z. Hussain, D. L. Church, D. B. Gregson, T. Louie, J. M. Conly, “New quadriplex PCR assay for detection of methicillin resistance and simultaneous discrimination of S. aureus from coagulase-negative Staphylococci,” Journal Clinical Microbiology, vol. 42, no. 11, pp. 4947-4955, 2004.
  • [29] J. A. McClure, J. M. Conly, V. Lau, S. Elsayed, T. Louie, W. Hutchins, K. Zhang, “Novel multiplex PCR assay for detection of the Staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from resistant Staphylococci,” Journal Clinical Microbiology, vol. 44, no. 3, pp. 1141-1144, 2006.
  • [30] P. Vasudevan, M. K. M. Nair, T. Annamalai, K. S. Venkitanarayanan, “Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation,” Veterinary Microbiology, vol. 92, no. 1-2, pp.179-185, 2003.
  • [31] Clinical laboratory standart institute, (CLSI), “Performance Standards for antimicrobial susceptibility testing. Twentieth edition,” Informational Supplement M100-S22, Wayne, PA, 2012.
  • [32] T. Saba, M. Sajid, A. A. Khan, R. Zahra, “Role of intracellular adhesion icaAD and agr genes in biofilm formation in clinical S. aureus isolates and assessment of two phenotypic methods,” Pakistan Journal of Medical Science, vol. 34, no. 3, pp. 633-637, 2018.
  • [33] K. Kolodziejczak, A. Onopiuk, A. Szpicer, A. Poltorak, “Meat analogues in the perspective of recent scientific research: a review,” Foods, vol. 11, no. 1, pp. 105, 2022.
  • [34] L. Grispoldi, P. A. Popescu, M. Karama, V. Gullo, G. Poerio, E. Borgogni, P. Torlai, G. Chianese, A. G. Fermani, P. Sechi, B. Cenci-Goga, “Study on the growth and enterotoxin production by Staphylococcus aureus in canned meat before retorting,” Toxins, vol. 11, no. 5, pp. 291, 2019.
  • [35] T. Thwala, E. Madoroba, A. Basson, P. Butaye, “Prevalence and characteristics of Staphylococcus aureus associated with meat and meat products in African countries: a review,” Antibiotics, vol. 10, no. 9, pp. 1108, 2021.
  • [36] E. O. Igbinosa, A. Beshiru, I. H. Igbinosa, A. G. Ogofure, T. C. Ekundayo, A. I. Okoh, “Prevalence, multiple antibiotic resistance and virulence profile of methicillin resistant Staphylococcus aureus (MRSA) in retail poultry meat from Edo, Nigeria,” Frontiers in Cellular and Infection Microbiology, vol. 13, pp. 1122059, 2023.
  • [37] D. Komodromos, C. Kotzamanidis, V. Giantzi, S. Pappa, A. Papa, A. Zdragas, A. Angelidis, D. Sergelidis, “Prevalence, infectious characteristics and genetic diversity of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) in two raw-meat processing establishments in Northern Greece,” Pathogens, vol. 11, no. 11, pp. 1370, 2022.
  • [38] M. Rajaei, M. H. Moosavy, S. N. Gharajalar, S. A. Khatibi, “Antibiotic resistance in the pathogenic foodborne bacteria isolated from raw kebab and hamburger: phenotypic and genotypic study,” BMC Microbiology, vol. 21, pp. 272, 2021.
  • [39] E. Keyvan, H. Özdemir, “Sığır karkaslarında Staphylococcus aureus’un varlığı, enterotoksijenik özellikleri ve antimikrobiyal dirençliliği,” Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 63, pp. 17-23, 2016.
  • [40] N. Gündoğdu, A. Devren, “Protease and lipase activity of Staphylococcus aureus obtained from meat, chicken and meatball samples,” Gazi University Journal of Science, vol. 23, no. 4, pp. 381-384, 2010.
  • [41] M. H. Chaia, T. A. M. Faiqa, S. M. Z. Ariffinb, Z. Suhailia, M. Z. Sukimana, M. F. Ghazali, “Prevalence of methicillin resistant Staphylococcus aureus in raw goat milks from selected farms in Terengganu, Malaysia,” Tropical Animal Science Journal, vol. 43, no. 1, pp. 64-69, 2020.
  • [42] A. M. Edris, A. A. A. Maarouf, R. A. E. Amin, E. A. I. Bahbah, “Prevalence of Staphylococci in meat products with special reference to methicillin-resistant Staphylococcus aureus (MRSA) at Kaliobia Governorate,” Benha Veterinary Medical Journal, vol. 35, no. 2, pp. 364-374, 2018.
  • [43] G. A. Ballash, A. L. Albers, D. F. Mollenkopf, E. Sechrist, R. J. Adams, T. E. Wittum, “Antimicrobial resistant bacteria recovered from retail ground meat products in the US include a Raoultella ornithinolytica co-harboring blaKPC-2 and blaNDM-5,” Scientific Reports, vol. 11, pp. 14041, 2021.
  • [44] S. Wu, J. Huang, Q. Wu, J. Zhang, F. Zhang, X. Yang, H. Wu, H. Zeng, M. Chen, Y. Ding, J. Wang T. Lei, S. Zhang, L. Xue, “Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity,” Frontiers in Microbiology, vol. 9, pp. 2767, 2018.
  • [45] M. G. Basanisi, G. La Bella, G. Nobili, S. Tola, M. A. Cafiero, G. La Salandra, “Prevalence and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from retail meat in south Italy,” Italian Journal of Food Science, vol. 32, no. 2, pp. 410-419, 2020.
  • [46] Z. T. Baghbaderani, A. Shakerian, E. Rahimi, “Phenotypic and genotypic assessment of antibiotic resistance of Staphylococcus aureus bacteria isolated from retail meat,” Infection and Drug Resistance, vol. 13, pp. 1339-1349, 2020.
  • [47] D. A. Hasanpour, L. Khaji, S. M. Sakhaei, Z. Mashak, D. F. Safarpoor, Y. Safaee, A. Hosseinzadeh, I. Alavi, E. Ghasem, F. M. Rabiei, “One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat,” Tropical Biomedicine, vol. 34, no. 2, pp. 396-404, 2017.
  • [48] P. Fowoyo, S. Ogunbanwo, “Antimicrobial resistance in coagulase-negative Staphylococci from Nigerian traditional fermented foods,” Annals of Clinical Microbiology and Antimicrobial, vol. 16, no. 4, pp. 1-7, 2017.
  • [49] A. Kılıç, E. Doğan, S. Kaya, M. Baysallar, “Yedi yıllık sürede klinik örneklerden izole edilen Staphylococcus aureus suşlarında mecC ve Panton-Valantine lökosidin gen varlığının araştırılması,” Mikrobiyoloji Bülteni, vol. 49, no. 4, pp. 594-599, 2015.
  • [50] R. Parastan, M. Kargara, K. Solhjooc, F. Kafilzadeh, “Staphylococcus aureus biofilms: structures, antibiotic resistance, inhibition, and vaccines,” Gene Reports, vol. 20, pp. 100739, 2020.
  • [51] A. C. Silva-de-Jesus, R. G. Ferrari, P. Panzenhagen, C. A. ConteJunior, “Staphylococcus aureus biofilm: the role in disseminating antimicrobial resistance over the meat chain,” Microbiology, vol. 168, pp. 001245, 2022.
  • [52] L. E. Alcaraz, S. E. Satorres, R. M. Lucero, O. N. P. Centorbi, “Species identification, slime production and oxacillin susceptibility in coagulase-negative staphylococci isolated from nosocomial specimens,” Brazilian Journal of Microbiology, vol. 34, no. 1, pp. 45-51, 2003.
  • [53] A. Ciftci, A. Findik, E. E. Onuk, S. Savasan, “Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis,” Brazilian Journal of Microbiology, vol. 40, no. 2, pp. 254-261, 2009.
  • [54] A. Prenafeta, M. Sitjà, M. A. Holmes, G. K. Paterson, “Communication: Biofilm production characterization of mecA and mecC methicillin-resistant Staphylococcus aureus isolated from bovine milk in Great Britain,” Journal of Dairy Science, vol. 97, pp. 4838–4841, 2014.
  • [55] A. E. M. A. Morshdy, A. E. Tharwat, A. M. A. Merwad, N. A. M. Abdallah, T. Saber, “Prevalence, phenotypic-genotypic resistance and biofilm formation of Staphylococcus aureus in chicken meat with reference to its public health hazard,” Veterinary Medicine and The One Health Concept, vol. 60, pp. 413–424, 2023.
  • [56] M. E. A. Bissong, C. N. Ateba, “Genotypic and phenotypic evaluation of biofilm production and antimicrobial resistance in Staphylococcus aureus isolated from milk, NorthWest province, South Africa,” Antibiotics, vol. 9, pp. 156, 2020.
  • [57] M. G. Avila-Novoa, M. Iñıguez-Moreno, O. A. Solıs-Velazquez, J. P. Gonzalez-Gomez, P. J. Guerrero-Medina, M. Gutierrez-Lomel, “Biofilm Formation by Staphylococcus aureus isolated from Food Contact Surfaces in the Dairy Industry of Jalisco, Mexico,” Journal of Food Quality, vol. 2018, pp. 1746139, 2018.
Toplam 57 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Yapısal Biyoloji
Bölüm Araştırma Makalesi
Yazarlar

Tuğba Sarı Bu kişi benim 0009-0006-9166-4647

Ceren Baskan 0000-0001-7849-4459

Erken Görünüm Tarihi 6 Haziran 2024
Yayımlanma Tarihi 30 Haziran 2024
Gönderilme Tarihi 15 Ekim 2023
Kabul Tarihi 13 Mart 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 28 Sayı: 3

Kaynak Göster

APA Sarı, T., & Baskan, C. (2024). Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs. Sakarya University Journal of Science, 28(3), 505-516. https://doi.org/10.16984/saufenbilder.1376028
AMA Sarı T, Baskan C. Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs. SAUJS. Haziran 2024;28(3):505-516. doi:10.16984/saufenbilder.1376028
Chicago Sarı, Tuğba, ve Ceren Baskan. “Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus Aureus Isolated from Ground Beef and Meatballs”. Sakarya University Journal of Science 28, sy. 3 (Haziran 2024): 505-16. https://doi.org/10.16984/saufenbilder.1376028.
EndNote Sarı T, Baskan C (01 Haziran 2024) Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs. Sakarya University Journal of Science 28 3 505–516.
IEEE T. Sarı ve C. Baskan, “Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs”, SAUJS, c. 28, sy. 3, ss. 505–516, 2024, doi: 10.16984/saufenbilder.1376028.
ISNAD Sarı, Tuğba - Baskan, Ceren. “Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus Aureus Isolated from Ground Beef and Meatballs”. Sakarya University Journal of Science 28/3 (Haziran 2024), 505-516. https://doi.org/10.16984/saufenbilder.1376028.
JAMA Sarı T, Baskan C. Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs. SAUJS. 2024;28:505–516.
MLA Sarı, Tuğba ve Ceren Baskan. “Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus Aureus Isolated from Ground Beef and Meatballs”. Sakarya University Journal of Science, c. 28, sy. 3, 2024, ss. 505-16, doi:10.16984/saufenbilder.1376028.
Vancouver Sarı T, Baskan C. Investigation of Biofilm Production and Determination of Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Ground Beef and Meatballs. SAUJS. 2024;28(3):505-16.

30930 This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.